Advances in Infectious Diseases, 2013, 3, 10-16
http://dx.doi.org/10.4236/aid.2013.31002 Published Online March 2013 (http://www.scirp.org/journal/aid)
Patient Demographics and Characteristics of Infection
with Carbapenem-Resistant Acinetobacter baumannii in a
Teaching Hosp i ta l fr om t he United States*
Nachiket D. Vaze, Christopher L. Emery, Richard J. Hamilton, Ari D. Brooks, Suresh G. Joshi#
Surgical & Nosocomial Infection Research and Bacterial Pathogenesis Program, Drexel University College of Medicine, Hahnemann
University Hospital, Philadelphia, USA
Email: #Suresh.Joshi@drexelmed.edu
Received November 13th, 2012; revised December 15th, 2012; accepted January 18th, 2013
ABSTRACT
A characterization of the clinical demographic features of patients with infection caused Acinetobacter baumannii, and
the antibiotyping of the isolates recovered from these patients was undertaken, with a special reference to carbapenem-
resistant variants, and their risk factors. This study was conducted retrospectively from January 2010 to March 2011 at a
616-bed tertiary care university hospital. Sixty-four patients were identified. Clinical and microbiological data were
analyzed for risk factors and demographic features to derive relative risk and odds ratio. We identified 100 A. bauman-
nii from 64 patients during 15 months period. Significant risk factors were working age (18 - 60 years), male gender,
hospital stay (>1 week but <1 month), prior hospitalization, in a progressive care nursing units, respiratory/mechanical
ventilation, polymicrobial infections and prior antibiotic therapy. Methicillin-resistant staphylococcus aureus (MRSA),
Pseudomonas aeruginosa, and Klebsiella pneumoniae were the significant co-infecting agents. The antibiogram dem-
onstrated multidrug resistance in a majority of the isolates. Relative risk associated with ventilator, diabetes, and sur-
gery was higher in repeat isolates than in first isolates and were multidrug resistant. Repeat isolates were more resistant
that the first isolates to most anti-acinetobacter agents, but the overall crude mortality was not significant during this
study period, and couldn’t correlated to the choice of treatment. In conclusion, a resistance against all clinically used
carbapenems, and colistin is rapidly increasing in repeat isolates of A. baumannii; leaves narrow therapeutic options to
treat multidrug-resistant and pandrug-resistant A. baumannii infection. For the first time we report rising incidence of
colistin resistance by 20 percent in repeat isolates, and is worrisome for healthcare centers. A combination therapy
should be adopted to treat such infection to avoid the emergence of colistin-resistant phenotypes in the United States.
Keywords: Acinetobacter ba um anni i ; Carbapenem Resistance; Colistin, Imipenem; Meropenem; Multidrug Resistance;
Risk Factor
1. Introduction
Acinetobacter baumannii is a third most prevalent noso-
comial pathogenic species. It has been isolated from
various hospital environments and has been shown to
colonize patients. Until recently, this pathogen was found
primarily outside the United States, mainly in Europe and
Asia [1,2], but it is emerging in the United States [3]. In
addition, A. baumann ii infections have been identified in
troops returning from military engagements in the Mid-
dle East [4]. A. baumannii has been identified as the cau-
sative agent in many serious medical conditions such as
sepsis and nosocomial pneumonia [5,6]. Although in
general the virulence of this species is low; its coloniza-
tion poses a threat in a health care setting. Pneumonia
caused by A. baumannii is associated with contaminated
or colonized surgical and respiratory equipment. Out-
breaks of A. baumannii have been reported in hospitals;
especially in intensive care units (ICUs) [7]. Its status as
an opportunistic organism makes it an unpredictable no-
socomial pathogen that can cause significant mortality in
such cases [8-10].
A. baumannii is inherently resistant to many antim-
icrobials and can further acquire resistance to additional
antimicrobials to become multidrug resistant (MDR).
MDR- A. ba umannii is a major cause of concern in heal-
th care settings, and the infections are extremely difficult
to treat [11,12]. MDR- A. baumannii is usually treated
with broad-spectrum antibiotics, including carbapenems.
Carbapenems such as imipenem and meropenem are of-
ten the antibiotics of last resort for such infection, and
*All authors report no conflict of interest related to this manuscript.
#Corresponding author.
Copyright © 2013 SciRes. AID
Patient Demographics and Characteristics of Infection with Carbapenem-Resistant Acinetobacter baumannii in
a Teaching Hospital from the United States
11
resistance against them is considered an alarming situa-
tion [13,14]. Many risk factors are associated with the
prevalence of A. baumannii and the development of MDR-
A. baumannii [15]. Environmental risk factors such as
intubation [16], prior surgery [17], and length of stay in
the ICU [18] can lead to the development of MDR in A.
baumannii.
In this study, the sensitivity of the isolates to imipe-
nem and meropenem was determined; imipenem-resis-
tant and meropenem-resistant isolates were further ana-
lyzed for the presence of risk factors. One of the major
reasons for antibiotic resistance is the persistence of in-
fection and recolonization with the variants that can lead
to repeat isolation of the same strain or a related strain
[19]. This phenomenon was also analyzed in the present
study. The repeat isolates are often much more virulent
and more likely to be MDR [20,21]. Because obtaining
repeat isolates is specifically related to hospital environ-
ments and therapy, a risk analysis was performed on
these isolates for resistance to imipenem and merope-
nem.
2. Materials, Methodology, and Set up
The study was conducted during Jun 2010 through Dec
2011 at a 616 bed tertiary care university hospital. Pa-
tients with Acinetobacter-positive cultures were identi-
fied from the microbiology laboratory database, and the
cases of A. baumannii infection were considered. The
isolates were identified using standard microbiological
laboratory tests and the API 20E and VITEK systems
(bioMérieux, Durham, NC). Antibiotic susceptibility data
were obtained using the VITEK 2 system (bioMérieux)
and minimum inhibitory concentrations (MICs) carried
out using agar microdilution technique, following the
Clinical and Laboratory Standards Institute (CLSI) gui-
delines. For each patient and each sample, clinical data
were accessed through the hospital online patient data-
base. The criterion for infection versus colonization was
interpreted as per Center for Disease Control and Preven-
tion (CDC) guidelines [22]. The isolate was considered
as multidrug resistant, if resistant to more than two class-
es of antimicrobials or to carbapenems. The first isolate
was defined as the organism that was first isolated from
the sample during hospital admission and the repeat iso-
late as the one that was obtained from the same patient
after the isolation of the first isolate (usually after an in-
terval of a week). Statistical analysis was carried out us-
ing GraphPad version 3.0 (GraphPad Software, LaJolla,
CA). Fisher’s exact test was applied, and odds ratios (OR)
and risk ratios (RR) with 95% confidence interval (CI)
values were calculated. A P value < 0.05 was considered
significant.
3. Results
Total 100 isolates were recovered from 64 cases of infec-
tion with A. baumannii were considered, having distinct
episodes of hospitalization. Table 1 demonstrates analy-
sis of the demographic features. The patients were group-
ed into two broad categories according to age to enable
comparison for analysis. Patients of working age (18 - 60
years) had a significantly higher chance of A. baumannii
infection than seniors (65 and older). More men than
women had infections with A. baumannii (OR = 2.78; CI
= 1.36 - 5.68; P = 0.0078). There was significant associa-
tion between a stay in the hospital of less than 1 month
but longer than 1 week and isolation of A. baumannii
compared to a longer stay in the hospital (OR = 3.51, CI
= 1.71 - 7.20; P = 0.0009). However, there was no sig-
nificant correlation between the samples collected during
the hospital stay, and culture positivity in regard to rela-
tive risk.
A source of sample is the important epidemiological
indicator. Almost half (49%) of the isolates were from
sputum and tracheal secretion; 36 (73%) of the patients
with A. baumannii isolated from sputum were on a me-
chanical ventilator. Sputum was a more likely source of
A. baumannii infection than bronchial wash (OR = 12.76,
CI = 5.39 - 30.24; P = 0.0001). Most of the samples col-
lected from ventilated patients had at least one other
bacterium. The most prevalent co-isolated organisms
were P. aeruginosa (25%) and methicillin-resistant S. au-
reus (19%) (Data is not shown).
The isolates were tested using the VITEK 2 system for
susceptibility against commonly used antibiotics and ca-
tegorized as resistant and susceptible groups according to
the results, interpreted as per the CLSI criteria. Figure 1
is a graphical presentation of antibiogram using common
antimicrobial agents, and indicates high levels of resis-
tance across drug classes. More than 50% of the isolates
were resistant to seven different antibiotics. Levofloxacin
was the most ineffective antibiotic. Even a combination
of piperacillin-tazobactam was ineffective. Both imipe-
nem and meropenem showed resistance to 44% and 49%
of the isolates, respectively. The only antibiotics that
were relatively effective against A. baumannii infections
were amikacin and colistin, and showed 30% and 11% of
the isolates as resistant phenotypes (respectively), during
studies of first isolates. Total 36 repeat isolates were in-
cluded in this study. Some patients had no repeat isolates
whereas some cases had more than two. A separate anal-
ysis was performed on these two groups, and their anti-
biogram and risk factor analysis were compared. The
comparison demonstrates an increase in resistance in the
repeat isolates against almost all antibiotics tested (Fig-
ure 1). The levels of resistance have increased by 30%
for levofloxacin, by 32% for trimethoprim-sulfamethoxa-
Copyright © 2013 SciRes. AID
Patient Demographics and Characteristics of Infection with Carbapenem-Resistant Acinetobacter baumannii in
a Teaching Hospital from the United States
Copyright © 2013 SciRes. AID
12
Table 1. Clinical demographic characteristics of Acinetobacter baumannii infections.
Characteristic Number of patients
(n = 64) Total (%)Groups to compare OR 95% CI RRP value
Age
18 to 40 years 18 28 Working group vs seniors6.01 2.82 - 13.0 2.50.0001
41 to 64 years 27 42
65 years and older 18 28
Infant 1 3
Gender
Female 24 37
Male 40 63
Male vs female 2.78 1.36 - 5.68 1.670.0078
Duration of hospital stay
Same-day discharge 4 6
1 week 15 23
More than 1 week but less than 1
month 26 39
More than 1 month 21 32 <1 month vs >1 month 3.51 1.71 - 7.20 1.950.0009
Characteristic Number of cases
(n = 100) Total (%) OR CI RRP value
Time to culture of samples
Day of admission 29 29
Less than 1 week of hospitalization 22 22
More than 1 week but less than 1
month 31 31
More than 1 month 18 18
Source of sample
Anerobe 9 9
Blood 10 10
Sputum vs blood 8.65 4.03 - 18.53 4.90.0001
Bronchi 7 7
Tissue 1 1
Urine 13 13
Wound 11 11
Sputum vs wound 7.77 3.71 - 16.28 4.450.0001
Sputum 49 49
Sputum vs bronchial wash12.76 5.39 - 30.24 7 0.0001
oxazole (Bactrim), and colistin to 22%. There was an
increase in the levels of resistance to imipenem (44% to
77%) and meropenem (49% to 71%).
Table 2 demonstrates the risk factor analysis for resis-
tance to carbapenem. Risk factors for resistant isolates
were determined through clinical data analysis, and the
odds ratios were calculated. Prior hospitalization was a
major risk factor for development of resistance to both
drugs. Significantly higher odds of developing a resistant
isolate were observed for carbapenem (OR = 5.56, CI =
2.7 - 11.47; P 0.05). Samples from the ventilated pa-
tients had an odds ratio of 1.9 for resistance to carba-
penem (OR = 1.9, CI = 1.01 - 3.52; P 0.05). A greater
number of resistant samples were taken from patients
who were hospitalized for less than a month compared to
patients with longer hospital stays (OR = 3.58, CI = 1.78
- 7.2; P 0.05). Sputum samples did not have a statisti-
cally significant risk for development of resistance to
either carbapenem. Diabetes was not associated with risk
of resistance in this analysis. Carbapenem here includes
Patient Demographics and Characteristics of Infection with Carbapenem-Resistant Acinetobacter baumannii in
a Teaching Hospital from the United States
13
59
62
57
51
49
46
44
37
29
30
0
89
65
76
83
71
78
77
71
47
30
22
0
10
20
30
40
50
60
70
80
90
100
Levofloxacin
Piperacilin/Tazobactam
Cefepime
Trimeth-Sulfametho
Meropenem
Gentamicin
Imipenem
Tobramycin
Ampicillin/Sulbact
Amikacin
C olis tin
Resistant Isolates (%)
Antimicrobial agents
Figure 1. A comparative antibiogram of the first and repeat (second) isolates (white bar, first isolates, n = 64; black bar, re-
peat isolate, n = 36).
Table 2. Risk factor analysis for carbapenem*.
Risk Factor Resistant Susceptible OR CI RR P value
Prior hospitalization 43 25 5.562.70 - 11.47 3.58 <0.05
Less than 1 month of hospitalization 43 38 3.581.78 - 7.20 2.8 <0.05
Polymicrobial infection 35 22 2.161.14 - 4.1 1.75 <0.05
Ventilator 36 27 1.9 1.01 - 3.52 1.65 <0.05
Sputum 26 22 0.8960.49 - 1.63 0.91 >0.05
Diabetes 19 11 0.4150.22 - 0.79 0.52 <0.05
*Carbapenem here includes imipenem and meropenem; and p values were similar on both cases.
imipenem and meropenem. A significance of risk factors
for both these agents are similar (P < 0.05), and separate
data is not shown.
A comparative study of the risk factors associated with
first and repeat isolates for carbapenem-resistance was
performed (Table 3). Association of the development of
resistance with certain risk factors was statistically sig-
nificant for repeat isolates. Although ventilator use was
Copyright © 2013 SciRes. AID
Patient Demographics and Characteristics of Infection with Carbapenem-Resistant Acinetobacter baumannii in
a Teaching Hospital from the United States
14
Table 3. First and repeat isolate comparison of risk factors for carbapenem*.
First Isolates Repeat Isolates
Risk Factor OR 95% CI RR P value OR 95% CI RR P value
Ventilator 1 0.45 - 2.23 1 >0.05 5.37 1.94 - 14.85 4.4 <0.05
Diabetes 1.18 0.53 - 2.63 1.15 >0.05 4.17 1.60 - 10.86 3.5 <0.05
Surgery NA NA NA NA 2.7 1.12 - 6.51 2.37 <0.05
*Carbapenem here includes imipenem and meropenem, and p values were similar in both cases.
not a significant factor for all isolates when considered
together, it significantly increased the odds of resistance
for repeat isolates for carbapenem (OR = 5.37, CI = 1.94
- 14.85; P 0.05). Diabetes, which was not seen as a
major factor for overall development of resistance, was a
risk factor for resistance development when studied re-
peat isolate from the specimen. This observation was
evident from the increase in the odds ratio and statistical
significance of the results (OR = 4.17, CI = 1.6 - 10.86; P
0.05). The risk factor was considered only when it was
applied to repeat isolates. Invasive procedures in the
hospital were considered for their association with the
resistant isolates. For the purpose of this study, debride-
ment, biopsies, and major surgeries were considered as
part of this category. Invasive procedures were an im-
portant risk factor for the development of resistance in
repeat isolates.
4. Discussion
The findings demonstrate the occurrence of Acinetobac-
ter infections in an urban hospital setting from the United
States. Analysis of the clinical data provided information
about the sources of the infections, with predominant risk
factors associated with identified Acinetobacter infec-
tions. Age has been discussed as a major factor associ-
ated with the acquisition of Acinetobacter [23]. Although
our sample size is smaller, a recent report on the analysis
of 55,000 US surveillance samples indicates that people
of working age have a higher risk of developing A.
baumannii than do elderly people [24]. Men had a rela-
tively higher risk of developing this infection. The higher
occurrence of A. baumannii infection in working men
could not be explained, but similar findings have been
reported from other countries [25]. Duration of hospi-
talization is an important factor associated with nosoco-
mial infections and hospital outbreaks. In the present
study, shorter stay (>1 week but <1 month) in the hospi-
tal contributed more to the incidence of infection. Prior
and prolonged hospitalization and antibiotic therapy are
established risk factors [10,18,26,27]. Therefore, the
finding is difficult to explain. The possibilities, such as
community acquisition or health care provider-associated
dissemination, remain to be demonstrated. Sputum was a
major source of A. baumannii, and the organism was
associated with ventilator-associated pneumonia [28] and
may indicate respiratory colonization and subsequent in-
vasion [29]. A. baumannii was also isolated in conjunc-
tion with other nosocomial pathogens such as methicil-
lin-resistant S. aureus and P. aeruginosa and denotes a
dangerous combination of polymicrobial infections, of-
fering more collective resistance.
Multidrug-resistant A. baumannii has been reported
worldwide. In the present study, the large-scale occur-
rence of MDR- A. baumannii indicates increased preva-
lence in urban US hospital. The carbapenem-resistant A.
baumannii isolates are increasingly reported from other
US hospitals too and narrows the therapeutic options to
control these superbugs. The large number of MDR- A.
baumannii isolates prompted us to determine and sys-
tematically analyze the associated risk factors. Common
risk factors suspected in previous studies [30], such as
patient’s time on a ventilator, were confirmed. The big-
gest risk factor for developing carbapenem-resistant A.
baumannii was prior hospitalization. This risk factor has
also been reported by other group [5] and could be in-
dicative of exposures in the hospital environment or of
the use of antibiotics that leads to development of resis-
tance. Samples from the patients on respiratory ventila-
tors and from those with polymicrobial infections [31]
also had high odds of developing carbapenem resistant A.
baumannii and suggest that cross contamination and co-
lonization of respiratory equipment could be a concern.
We also observed many repeat isolates among the total
isolates and risk factors associated with resistance among
them. Separate risk analysis between first and repeat iso-
lates indicated the association of certain risk factors that
were not significant in the overall analysis of all samples.
The risk of developing repeat isolate resistant to carbap-
enems increased significantly with ventilator use. Inva-
sive procedures have been associated with the multidrug
resistance [7]. Diabetes and prior surgery, which were
not significantly associated with overall resistance, were
major risk factors in developing resistance in a second
(or repeat) isolate. In our studies, many elderly patients
who were hospitalized had a sacral decubitus ulcer, and
Copyright © 2013 SciRes. AID
Patient Demographics and Characteristics of Infection with Carbapenem-Resistant Acinetobacter baumannii in
a Teaching Hospital from the United States
15
were subsequently found to be infected [32]. These pa-
tients had come for a debridement procedure. The majo-
rity of these patients were ventilated, but a clear correla-
tion could not be established in the acquisition of A.
baumannii. These patients are usually given broad-spec-
trum antibiotics to control infection and are sent back to
their long-term care facility and may be subsequently
contributing to dissemination of A. baumannii in such
health care facilities and the community at large. Further
follow-up is required in such cases to gain more insight.
We did not analyzed patient outcome and therapy evalua-
tion analysis, which are beyond the scope of the present
study. These analyses will require a manual data mining
as not all the documents are retrievable.
In conclusion, a multidrug resistance was observed in
a majority of the isolates. The repeat isolates displayed
an increased level of antibiotic resistance. The resistance
against all carbapenems and colistin is rapidly increasing;
and the resistance was double in many of the repeat
(second) isolates compared to initial (first) isolates against
colistin, the drug of choice for such infections. A combi-
nation therapy is strongly advisable against such infec-
tions to avoid the emergence of colistin-resistant pheno-
types in the United States hospitals.
5. Acknowledgements
This research work was partly supported by intramural
funds from Drexel University College of Medicine, and
partly, by the grant from Merck & Co. Authors thank Ms.
Pamela Fried for critical input in the manuscript. The
study has IRB approval from the Drexel University Col-
lege of Medicine.
REFERENCES
[1] M. Turkoglu, E. Mirza, O. G. Tunccan, et al., “Acineto-
bacter baumannii Infection in Patients with Hematologic
Malignancies in Intensive Care Unit: Risk Factors and
Impact on Mortality,” Journal of Critical Care, Vol. 26,
No. 5, 2011, pp. 460-467. doi:10.1016/j.jcrc.2011.04.007
[2] M. Shanthi and U. Sekar, “Multi-Drug Resistant Pseu-
domonas aeruginosa and Acinetobacter baumannii Infec-
tions among Hospitalized Patients: Risk Factors and Out-
comes,” Journal of the Association of Physicians of India,
Vol. 57, 2009, pp. 636-645.
[3] H. Wisplinghoff, T. Paulus, M. Lugenheim, et al., “Noso-
comial Bloodstream Infections Due to Acinetobacter
baumannii, Acinetobacter pittii and Acinetobacter noso-
comialis in the United States,” Journal of Infection, Vol.
64, No. 3, 2012, pp. 282-290.
doi:10.1016/j.jinf.2011.12.008
[4] T. J. Whitman, S. S. Qasba, J. G. Timpone, et al., “Occu-
pational Transmission of Acinetobacter baumannii from a
United States Serviceman Wounded in Iraq to a Health
Care Worker,” Clinical Infectious Diseases, Vol. 47, No.
4, 2008, pp. 439-443. doi:10.1086/589247
[5] M. Dizbay, O. G. Tunccan, B. E. Sezer, et al., “Nosoco-
mial Imipenem-Resistant Acinetobacter baumannii Infec-
tions: Epidemiology and Risk Factors,” Scandanavian
Journal of Infectious Diseases, Vol. 42, No. 10, 2010, pp.
741-746. doi:10.3109/00365548.2010.489568
[6] J. Gomez, E. Simarro, V. Banos, et al., “Six-Year Pro-
spective Study of Risk and Prognostic Factors in Patients
with Nosocomial Sepsis Caused by Acinetobacter bau-
mannii,” European Journal Clinical Microbiology and
Infectious Diseases, Vol. 18, No. 5, 1999, pp. 358-361.
doi:10.1007/PL00015019
[7] J. Y. Jung, M. S. Park, S. E. Kim, et al., “Risk Factors for
Multi-Drug Resistant Acinetobacter baumannii Bactere-
mia in Patients with Colonization in the Intensive Care
Unit,” BMC Infectious Diseases, Vol. 10, 2010, p. 228.
doi:10.1186/1471-2334-10-228
[8] S. Yang, H. J. Yoon and M. R. Ki, “Risk Factors for
Mortality in Acinetobacter bacteremia,” Brazilianl Jour-
nal of Infectious Diseases, Vol. 15, No. 5, 2011, pp. 501-
502.
[9] C. G. Prates, A. F. Martins, S. V. Superti, et al., “Risk
Factors for 30-Day Mortality in Patients with Carbap-
enem-Resistant Acinetobacter baumannii during an Out-
break in an Intensive Care Unit,” Epidemiology and In-
fection, Vol. 139, No. 3, 2011, pp. 411-418.
doi:10.1017/S0950268810001238
[10] S. G. Joshi, G. M. Litake, M. G. Satpute, et al., “Clinical
and Demographic Features of Infection Caused by Acine-
tobacter Species,” Indian Journal of Medical Sciences,
Vol. 60, No. 9, 2006, pp. 351-360.
doi:10.4103/0019-5359.27219
[11] M. del Mar Tomas, M. Cartelle, S. Pertega, et al., “Hos-
pital Outbreak Caused by a Carbapenem-Resistant Strain
of Acinetobacter baumannii: Patient Prognosis and Risk-
Factors for Colonisation and Infection,” Clinical Micro-
biology and Infection, Vol. 11, No. 7, 2005, pp. 540-546.
doi:10.1111/j.1469-0691.2005.01184.x
[12] S. F. Beavers, D. B. Blossom, T. L. Wiemke, et al.,
“Comparison of Risk Factors for Recovery of Acineto-
bacter baumannii during Outbreaks at Two Kentucky
Hospitals, 2006,” Public Health Reports, Vol. 124, No. 6,
2009, pp. 868-874.
[13] J. M. Cisneros, J. Rodriguez-Bano, F. Fernandez-Cuenca,
et al., “Risk-Factors for the Acquisition of Imipenem-
Resistant Acinetobacter baumannii in Spain: A Nation-
wide Study,” Clinical Microbiology and Infection, Vol.
11, No. 11, 2005, pp. 874-879.
doi:10.1111/j.1469-0691.2005.01256.x
[14] Y. S. Park, H. Lee, K. S. Lee, et al., “Extensively Drug-
Resistant Acinetobacter baumannii: Risk Factors for Ac-
quisition and Prevalent OXA-Type Carbapenemases: A
Multicentre Study,” International Journal of Antimicro-
bial Agents, Vol. 36, No. 5, 2010, pp. 430-435.
doi:10.1016/j.ijantimicag.2010.06.049
[15] Y. J. Kim, S. I. Kim, Y. R. Kim, et al., “Carbapenem-
Resistant Acinetobacter baumannii: Diversity of Resistant
Mechanisms and Risk Factors for Infection,” Epidemiol-
Copyright © 2013 SciRes. AID
Patient Demographics and Characteristics of Infection with Carbapenem-Resistant Acinetobacter baumannii in
a Teaching Hospital from the United States
Copyright © 2013 SciRes. AID
16
ogy and Infection, Vol. 140, No. 1, 2012, pp. 137-145.
doi:10.1017/S0950268811000744
[16] J. Baraibar, H. Correa, D. Mariscal, et al., “Risk Factors
for Infection by Acinetobacter baumannii in Intubated
Patients with Nosocomial Pneumonia,” Chest, Vol. 112,
No. 4, 1997, pp. 1050-1054.
doi:10.1378/chest.112.4.1050
[17] T. H. Wong, B. H. Tan, M. L. Ling, et al., “Multi-Resis-
tant Acinetobacter baumannii on a Burns Unit: Clinical
Risk Factors and Prognosis,” Burns, Vol. 28, No. 4, 2002,
pp. 349-357. doi:10.1016/S0305-4179(02)00012-8
[18] W. H. Sheng, C. H. Liao, T. L. Lauderdale, et al., “A
Multicenter Study of Risk Factors and Outcome of Hos-
pitalized Patients with Infections Due to Carbapenem-
Resistant Acinetobacter baumannii,” International Jour-
nal of Infectious Diseases, Vol. 14, No. 9, 2010, pp.
764-769. doi:10.1016/j.ijid.2010.02.2254
[19] M. M. D’Andrea, C. Venturelli, T. Giani, et al., “Persis-
tent Carriage and Infection by Multidrug-Resistant Es-
cherichia Coli ST405 Producing NDM-1 Carbapenemase:
Report on the First Italian Cases,” Journal of Clinical
Microbiology, Vol. 49, No. 7, 2011, pp. 2755-2758.
doi:10.1128/JCM.00016-11
[20] R. Jayaraman, “Hypermutation and Stress Adaptation in
Bacteria,” Journal of Genetics, Vol. 90, No. 2, 2011, pp.
383-391. doi:10.1007/s12041-011-0086-6
[21] J. D. Pitout, K. B. Laupland, D. L. Church, et al., “Viru-
lence Factors of Escherichia Coli Isolates that Produce
CTX-M-Type Extended-Spectrum Beta-Lactamases,” An-
timicrobial Agents and Chemotherapy, Vol. 49, No. 11,
2005, pp. 4667-4670.
doi:10.1128/AAC.49.11.4667-4670.2005
[22] J. Rodriguez-Bano, J. M. Cisneros, F. Fernandez-Cuenca,
et al., “Clinical Features and Epidemiology of Acineto-
bacter baumannii Colonization and Infection in Spanish
Hospitals,” Infect Control and Hospital Epidemiology,
Vol. 25, No. 10, 2004, pp. 819-824.
doi:10.1086/502302
[23] S. M. Poutanen, M. Louie and A. E. Simor, “Risk Factors,
Clinical Features and Outcome of Acinetobacter bactere-
mia in Adults,” European Journal of Clinical Microbiol-
ogy and Infectious Diseases, Vol. 16, No. 10, 1997, pp.
737-740. doi:10.1007/BF01709254
[24] R. M. Mera, L. A. Miller, H. Amrine-Madsen, et al.,
Acinetobacter baumannii 2002-2008: Increase of Car-
bapenem-Associated Multiclass Resistance in the United
States,” Microbial Drug Resistance, Vol. 16, No. 3, 2010,
pp. 209-215. doi:10.1089/mdr.2010.0052
[25] A. Abbo, S. Navon-Venezia, O. Hammer-Muntz, et al.,
“Multidrug-Resistant Acinetobacter baumannii,” Emerg-
ing Infectious Diseases, Vol. 11, No. 1, 2005, pp. 22-29.
doi:10.3201/eid1101.040001
[26] G. Baran, A. Erbay, H. Bodur, et al., “Risk Factors for
Nosocomial Imipenem-Resistant Acinetobacter bauman-
nii Infections,” International Journal of Infectious Dis-
eases, Vol. 12, No. 1, 2008, pp. 16-21.
doi:10.1016/j.ijid.2007.03.005
[27] N. Y. Lee, H. C. Lee, N. Y. Ko, et al. , “Clinical and Eco-
nomic Impact of Multidrug Resistance in Nosocomial
Acinetobacter baumannii Bacteremia,” Infection Control
and Hospital Epidemiology, Vol. 28, No. 6, 2007, pp.
713-719. doi:10.1086/517954
[28] J. Medina, C. Formento, J. Pontet, et al., “Prospective
Study of Risk Factors for Ventilator-Associated Pneumo-
nia Caused by Acinetobacter Species,” Journal of Critical
Care, Vol. 22, No. 1, 2007, pp. 18-26.
doi:10.1016/j.jcrc.2006.06.010
[29] A. Martinez-Pellus, J. Ruiz Gomez, F. Jaime Sanchez, et
al., “[Incidence of Colonization and Infection by Acine-
tobacter baumannii in an Endemic Seting (ICU). Analy-
sis of Risk Factors by Means of a Surveillance Study],”
Enfermedades Infecciosas y Microbiologia Clinica, Vol.
20, No. 5, 2002, pp. 194-199.
[30] H. C. Chang, Y. C. Chen, M. C. Lin, et al., “Mortality
Risk Factors in Patients with Acinetobacter baumannii
Ventilator: Associated Pneumonia,” Journal of the For-
mosan Medical Association, Vol. 110, No. 9, 2011, pp.
564-571. doi:10.1016/j.jfma.2011.07.004
[31] P. A. Tilley and F. J. Roberts, “Bacteremia with Acine-
tobacter Species: Risk Factors and Prognosis in Different
Clinical Settings,” Clinical Infectious Diseases, Vol. 18,
No. 6, 1994, pp. 896-900. doi:10.1093/clinids/18.6.896
[32] J. Koprnova, I. Svetlansky, R. Babel’a, et al., “Prospec-
tive Study of Antibacterial Susceptibility, Risk Factors
and Outcome of 157 Episodes of Acinetobacter bauman-
nii Bacteremia in 1999 in Slovakia,” Scandanavian Jour-
nal of Infectious Diseases, Vol. 33, No. 12, 2001, pp.
891-895. doi:10.1080/00365540110076688
Abbreviations
ICU: Intensive care unit;
MRSA: Methicillin-resistant Staphylococcus aureus;
M
DR: Multi drug resistance;
MIC: Minimum inhibitory concentration;
OR: Odds ratio;
RR: Relative risk;
CI: Confidence interval.